Gulls living in cities as overlooked seed dispersers within and outside urban environments.

The yellow-legged gull is an opportunistic and generalist bird that has colonised urban areas, where it has found very favourable trophic resources but also causes disturbance to humans and damage to infrastructure. Here, we investigated the potential role that gulls play in the dispersal of plants in Barcelona, a highly populated city of north-eastern Spain. We analysed the stomach contents of 145 chicks collected in urban nests and reported the presence of seeds of 27 plant taxa. We then developed a plant dispersal model based on the movements of 20 GPS-tracked yellow-legged gulls breeding in the city of Barcelona. We estimated seed dispersal distances, seed shadows and percentage of seeds reaching habitats suitable for seeds regurgitated in pellets and those excreted in faeces. Seven of the 27 plant taxa found in the stomachs were alien taxa to Spain. Average dispersal distances of plant seeds by gulls were around 700 m, but maximum dispersal distances reached up to 35 km. Dispersal distances and seed spatial patterns did not differ between faeces and pellet models, as most strongly depended on gull movements. About 95% of the seeds were dispersed within urban environments and between 20 and 30% reached suitable habitats for seed deposition (urban woodlands, green urban parks and urban grasslands). Urban gulls frequently dispersed seeds (including alien species) within urban habitats, both via direct consumption or via secondary dispersal after consuming granivorous birds that had ingested the seeds, such as pigeons or parakeets. Urban planning for Barcelona is based on native plant species, and thus, special attention should be paid to alien plants dispersed by birds, which could pose a risk to native biodiversity in urban ecosystems.

First days at sea: depicting migration patterns of juvenile seabirds in highly impacted seascapes.

Increasing human activities have detrimental consequences on marine ecosystems and their impact can have cumulative effects. Within marine ecosystems, seabirds respond to ecosystem variability and face multiple human pressures, especially threatened species. In long-lived species, juveniles and immatures could represent up to 50% of the total population, but their migratory movements remain largely unknown. Here, we depict the migratory patterns of juvenile Balearic shearwaters Puffinus mauretanicus, the most threatened European seabird, using miniaturised satellite transmitters. At the end of the 2012 breeding season, five tagged juveniles left the breeding colonies of Eivissa Island (western Mediterranean) the first week of July. They moved westwards to reach the Atlantic Ocean between 3 and 13 days afterwards. Juveniles showed a two-phase migratory pattern: they first travelled slower close to the breeding colonies, and then moved towards their wintering areas in the Atlantic Ocean by rapid directional movements. Environmental cues (e.g.,marine productivity, water mass distribution, frontal systems) might have a prominent role in driving the migratory patterns of juvenile Balearic shearwaters, moving from warm and poor marine areas in the Mediterranean Sea to cooler and rich non-breeding grounds in the Atlantic Ocean. Based on observational findings, we observed certain spatial overlap of juvenile Balearic shearwaters with areas of high human impact, but the relationship between flying travel speed and both fishing effort and cumulative human impacts were not statistically significant. These results suggest that more research is needed to assess whether the movement patterns of migrating juveniles are affected by human activities. Therefore, understanding the at-sea spatial ecology of juveniles should be a priority for research and conservation due to the importance of this population component in long-lived species, as well as assessing their vulnerability to multiple anthropogenic pressures.

Author Correction: Sea ice phenology and primary productivity pulses shape breeding success in Arctic seabirds.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Humans shape the year-round distribution and habitat use of an opportunistic scavenger.

Research focused on evaluating how human food subsidies influence the foraging ecology of scavenger species is scarce but essential for elucidating their role in shaping behavioral patterns, population dynamics, and potential impacts on ecosystems. We evaluate the potential role of humans in shaping the year-round distribution and habitat use of individuals from a typical scavenger species, the yellow-legged gull (Larus michahellis), breeding at southwestern Spain. To do this, we combined long-term, nearly continuous GPS-tracking data with spatially explicit information on habitat types and distribution of human facilities, as proxied by satellite imagery of artificial night lights. Overall, individuals were mainly associated with freshwater habitats (mean proportion, 95% CI: 40.6%, 36.9%-44.4%) followed by the marine-related systems (40.3, 37.7%-42.8%), human-related habitats (13.5%, 13.2%-13.8%), and terrestrial systems (5.5%, 4.6%-6.5%). However, these relative contributions to the overall habitat usage largely changed throughout the annual cycle as a likely response to ecological/physiological constraints imposed by varying energy budgets and environmental constraints resulting from fluctuations in the availability of food resources. Moreover, the tight overlap between the year-round spatial distribution of gulls and that of human facilities suggested that the different resources individuals relied on were likely of anthropogenic origin. We therefore provide evidence supporting the high dependence of this species on human-related food resources throughout the annual cycle. Owing to the ability of individuals to disperse and reach transboundary areas of Spain, Portugal, or Morocco, international joint efforts aimed at restricting the availability of human food resources would be required to manage this overabundant species and the associated consequences for biodiversity conservation (e.g., competitive exclusion of co-occurring species) and human interests (e.g., airports or disease transmission).

Behavioral rhythms of an opportunistic predator living in anthropogenic landscapes.

BACKGROUND: Human activities have profoundly altered the spatio-temporal availability of food resources. Yet, there is a clear lack of knowledge on how opportunistic species adapt to these new circumstances by scheduling their daily rhythms and adjust their foraging decisions to predicable patterns of anthropic food subsidies. Here, we used nearly continuous GPS tracking data to investigate the adaptability of daily foraging activity in an opportunistic predator, the yellow-legged gull (Larus michahellis), in response to human schedules. METHODS: By using waveform analysis, we compared timing and magnitude of peaks in daily activity of different GPS-tracked individuals in eleven different habitat types, in relation to type of day (i.e., weekday vs. weekend). RESULTS: Daily activity rhythms varied greatly depending on whether it was a weekday or weekend, thus suggesting that gulls' activity peaks matched the routines of human activity in each habitat type. We observed for the first time two types of activity as modelled by waveforms analysis: marine habitats showed unimodal patterns with prolonged activity and terrestrial habitats showed bimodal patterns with two shorter and variable activity peaks. CONCLUSIONS: Our results suggest that gulls are able to fine-tune their daily activity rhythms to habitat-specific human schedules, since these likely provide feeding opportunities. Behavioral plasticity may thus be an important driver of expansive population dynamics. Information on predictable relationships between daily activity patterns of gulls and human activities is therefore relevant to their population management.

Pathogen transmission risk by opportunistic gulls moving across human landscapes.

Wildlife that exploit human-made habitats hosts and spreads bacterial pathogens. This shapes the epidemiology of infectious diseases and facilitates pathogen spill-over between wildlife and humans. This is a global problem, yet little is known about the dissemination potential of pathogen-infected animals. By combining molecular pathogen diagnosis with GPS tracking of pathogen-infected gulls, we show how this knowledge gap could be filled at regional scales. Specifically, we generated pathogen risk maps of Salmonella, Campylobacter and Chlamydia based on the spatial movements of pathogen-infected yellow-legged gulls (Larus michahellis) equipped with GPS recorders. Also, crossing this spatial information with habitat information, we identified critical habitats for the potential transmission of these bacteria in southern Europe. The use of human-made habitats by infected-gulls could potentially increase the potential risk of direct and indirect bidirectional transmission of pathogens between humans and wildlife. Our findings show that pathogen-infected wildlife equipped with GPS recorders can provide accurate information on the spatial spread risk for zoonotic bacteria. Integration of GPS-tracking with classical epidemiological approaches may help to improve zoonosis surveillance and control programs.

Maiden voyage into death: are fisheries affecting seabird juvenile survival during the first days at sea?

The study of juvenile migration behaviour of seabird species has been limited so far by the inability to track their movements during long time periods. Foraging and flying skills of young individuals are assumed to be inferior to those of adults, making them more vulnerable during long-distance migrations. In addition to natural oceanographic effects and intrinsic conditions, incidental seabird harvest by human fisheries is one of the main causes of worldwide seabird population declines, and it has been hypothesized that juveniles are particularly vulnerable to bycatch during their first weeks at sea after leaving the nest. We used solar-powered satellite tags to track the at-sea movements of adults and juveniles of Scopoli's shearwater (Calonectris diomedea) after the autumn departure from their breeding colony in Chafarinas Islands (southwestern Mediterranean Sea). Eighty per cent of juvenile tags stopped transmitting during the first week at sea, within 50 km of their natal colony, in an area with one of the highest concentrations of fishing activities in the Mediterranean Sea. All adult birds tagged and only 20% of juveniles migrated into the Atlantic and southwards along the coast of West Africa. The two age groups showed different habitat preferences, with juveniles travelling farther from the coast, in windier and less productive waters than adults. We conclude that Scopoli's shearwater juveniles are particularly vulnerable to mortality events, and we highlight that fisheries, along with differential age-related behaviour skills between adults and juveniles, are likely causes of this mortality. Overall, our study highlights the importance of conducting tracking studies during the first stages of juvenile migration.

An adaptive method for identifying marine areas of high conservation priority.

Identifying priority areas for biodiversity conservation is particularly challenging in the marine environment due to the open and dynamic nature of the ocean, the paucity of information on species distribution, and the necessary balance between marine biodiversity conservation and essential supporting services such as seafood provision. We used the Patagonian seabird breeding community as a case study to propose an integrated and adaptive method for delimiting key marine areas for conservation. Priority areas were defined through a free decision-support tool (Marxan) that included projected at-sea distributions of seabirds (approximately 2,225,000 individuals of 14 species); BirdLife Important Bird and Biodiversity Areas (IBAs) for pelagic bird species; and the economic costs of potential regulations in fishing practices. The proposed reserve network encompassed approximately 300,000 km2 that was largely concentrated in northern and southern inshore and northern and central offshore regions. This reserve network exceeded the minimum threshold of 20% conservation of the abundance of each species proposed by the World Parks Congress. Based on marine currents in the study area, we further identified the 3 primary water masses that may influence areas of conservation priority through water inflow. Our reserve network may benefit from enhanced marine productivity in these highly connected areas, but they may be threatened by human impacts such as marine pollution. Our method of reserve network design is an important advance with respect to the more classical approaches based on criteria defined for one or a few species and may be particularly useful when information on spatial patterns is data deficient. Our approach also accommodates addition of new information on seabird distribution and population dynamics, human activities, and alterations in the marine environment.

Seasonal and circadian biases in bird tracking with solar GPS-tags.

Global Positioning System (GPS) tags are nowadays widely used in wildlife tracking. This geolocation technique can suffer from fix loss biases due to poor satellite GPS geometry, that result in tracking data gaps leading to wrong research conclusions. In addition, new solar-powered GPS tags deployed on birds can suffer from a new "battery drain bias" currently ignored in movement ecology analyses. We use a GPS tracking dataset of bearded vultures (Gypaetus barbatus), tracked for several years with solar GPS tags, to evaluate the causes and triggers of fix and data retrieval loss biases. We compare two models of solar GPS tags using different data retrieval systems (Argos vs GSM-GPRS), and programmed with different duty cycles. Neither of the models was able to accomplish the duty cycle programed initially. Fix and data retrieval loss rates were always greater than expected, and showed non-random gaps in GPS locations. Number of fixes per month of tracking was a bad criterion to identify tags with smaller biases. Fix-loss rates were four times higher due to battery drain than due to poor GPS satellite geometry. Both tag models were biased due to the uneven solar energy available for the recharge of the tag throughout the annual cycle, resulting in greater fix-loss rates in winter compared to summer. In addition, we suggest that the bias found along the diurnal cycle is linked to a complex three-factor interaction of bird flight behavior, topography and fix interval. More fixes were lost when vultures were perching compared to flying, in rugged versus flat topography. But long fix-intervals caused greater loss of fixes in dynamic (flying) versus static situations (perching). To conclude, we emphasize the importance of evaluating fix-loss bias in current tracking projects, and deploying GPS tags that allow remote duty cycle updates so that the most appropriate fix and data retrieval intervals can be selected.

Sea ice phenology and primary productivity pulses shape breeding success in Arctic seabirds.

Spring sea ice phenology regulates the timing of the two consecutive pulses of marine autotrophs that form the base of the Arctic marine food webs. This timing has been suggested to be the single most essential driver of secondary production and the efficiency with which biomass and energy are transferred to higher trophic levels. We investigated the chronological sequence of productivity pulses and its potential cascading impacts on the reproductive performance of the High Arctic seabird community from Svalbard, Norway. We provide evidence that interannual changes in the seasonal patterns of marine productivity may impact the breeding performance of little auks and Brünnich's guillemots. These results may be of particular interest given that current global warming trends in the Barents Sea region predict one of the highest rates of sea ice loss within the circumpolar Arctic. However, local- to regional-scale heterogeneity in sea ice melting phenology may add uncertainty to predictions of climate-driven environmental impacts on seabirds. Indeed, our fine-scale analysis reveals that the inshore Brünnich's guillemots are facing a slower advancement in the timing of ice melt compared to the offshore-foraging little auks. We provide a suitable framework for analyzing the effects of climate-driven sea ice disappearance on seabird fitness.

Climate impacts on global hot spots of marine biodiversity.

Human activities drive environmental changes at scales that could potentially cause ecosystem collapses in the marine environment. We combined information on marine biodiversity with spatial assessments of the impacts of climate change to identify the key areas to prioritize for the conservation of global marine biodiversity. This process identified six marine regions of exceptional biodiversity based on global distributions of 1729 species of fish, 124 marine mammals, and 330 seabirds. Overall, these hot spots of marine biodiversity coincide with areas most severely affected by global warming. In particular, these marine biodiversity hot spots have undergone local to regional increasing water temperatures, slowing current circulation, and decreasing primary productivity. Furthermore, when we overlapped these hot spots with available industrial fishery data, albeit coarser than our estimates of climate impacts, they suggest a worrying coincidence whereby the world's richest areas for marine biodiversity are also those areas mostly affected by both climate change and industrial fishing. In light of these findings, we offer an adaptable framework for determining local to regional areas of special concern for the conservation of marine biodiversity. This has exposed the need for finer-scaled fishery data to assist in the management of global fisheries if the accumulative, but potentially preventable, effect of fishing on climate change impacts is to be minimized within areas prioritized for marine biodiversity conservation.

Feathered Detectives: Real-Time GPS Tracking of Scavenging Gulls Pinpoints Illegal Waste Dumping.

Urban waste impacts human and environmental health, and waste management has become one of the major challenges of humanity. Concurrently with new directives due to manage this human by-product, illegal dumping has become one of the most lucrative activities of organized crime. Beyond economic fraud, illegal waste disposal strongly enhances uncontrolled dissemination of human pathogens, pollutants and invasive species. Here, we demonstrate the potential of novel real-time GPS tracking of scavenging species to detect environmental crime. Specifically, we were able to detect illegal activities at an officially closed dump, which was visited recurrently by 5 of 19 GPS-tracked yellow-legged gulls (Larus michahellis). In comparison with conventional land-based surveys, GPS tracking allows a much wider and cost-efficient spatiotemporal coverage, even of the most hazardous sites, while GPS data accessibility through the internet enables rapid intervention. Our results suggest that multi-species guilds of feathered detectives equipped with GPS and cameras could help fight illegal dumping at continental scales. We encourage further experimental studies, to infer waste detection thresholds in gulls and other scavenging species exploiting human waste dumps.

Oceanographic drivers and mistiming processes shape breeding success in a seabird.

Understanding the processes driving seabirds' reproductive performance through trophic interactions requires the identification of seasonal pulses in marine productivity. We investigated the sequence of environmental and biological processes driving the reproductive phenology and performance of the storm petrel (Hydrobates pelagicus) in the Western Mediterranean. The enhanced light and nutrient availability at the onset of water stratification (late winter/early spring) resulted in annual consecutive peaks in relative abundance of phytoplankton, zooplankton and ichthyoplankton. The high energy-demanding period of egg production and chick rearing coincided with these successive pulses in food availability, pointing to a phenological adjustment to such seasonal patterns with important fitness consequences. Indeed, delayed reproduction with respect to the onset of water stratification resulted in both hatching and breeding failure. This pattern was observed at the population level, but also when confounding factors such as individuals' age or experience were also accounted for. We provide the first evidence of oceanographic drivers leading to the optimal time-window for reproduction in an inshore seabird at southern European latitudes, along with a suitable framework for assessing the impact of environmentally driven changes in marine productivity patterns in seabird performance.

Toward a Deuterium Feather Isoscape for Sub-Saharan Africa: Progress, Challenges and the Path Ahead.

A key challenge to the application of continent-wide feather isoscapes for geographic assignment of migrant birds is the lack of ground-truthed samples. This is especially true for long-distance Palearctic-Afrotropical migrants. We used spatially-explicit information on the δ2H composition of archived feathers from Green-backed/Grey-backed Camaroptera, to create a feather δ2H isoscape for sub-Saharan Africa. We sampled from 34 out of 41 sub-Saharan countries, totaling 205 sampling localities. Feather samples were obtained from museum collections (n = 224, from 1950 to 2014) for δ2H assay. Region, altitude, annual rainfall and seasonal patterns in precipitation were revealed as relevant explanatory variables for spatial patterns in feather δ2H. Predicted feather δ2H values ranged from -4.0 ‰ to -63.3 ‰, with higher values observed in the Great Rift Valley and South Africa, and lower values in central Africa. Our feather isoscape differed from that modelled previously using a precipitation δ2H isoscape and an assumed feather-to-precipitation calibration, but the relatively low model goodness fit (F10,213 = 5.98, p<0.001, R2 = 0.18) suggests that other, non-controlled variables might be driving observed geographic patterns in feather δ2H values. Additional ground-truthing studies are therefore recommended to improve the accuracy of the African feather δ2H isoscape.

A novel spatio-temporal scale based on ocean currents unravels environmental drivers of reproductive timing in a marine predator.

Life-history strategies have evolved in response to predictable patterns of environmental features. In practice, linking life-history strategies and changes in environmental conditions requires comparable space-time scales between both processes, a difficult match in most marine system studies. We propose a novel spatio-temporal and dynamic scale to explore marine productivity patterns probably driving reproductive timing in the inshore little penguin (Eudyptula minor), based on monthly data on ocean circulation in the Southern Ocean, Australia. In contrast to what occurred when considering any other fixed scales, little penguin's highly variable laying date always occurred within the annual peak of ocean productivity that emerged from our newly defined dynamic scale. Additionally, local sea surface temperature seems to have triggered the onset of reproduction, acting as an environmental cue informing on marine productivity patterns at our dynamic scale. Chlorophyll-a patterns extracted from this scale revealed that environment factors in marine ecosystems affecting breeding decisions are related to a much wider region than foraging areas that are commonly used in current studies investigating the link between animals' life history and their environment. We suggest that marine productivity patterns may be more predictable than previously thought when environmental and biological data are examined at appropriate scales.

Living on the edge: demography of the slender-billed gull in the Western Mediterranean.

Small and peripheral populations are typically vulnerable to local extinction processes but important for the metapopulation dynamics of species. The Slender-billed gull (Chroicocephalus genei) is a long-lived species breeding in unstable ephemeral coastal habitats. Their Western Mediterranean populations are relatively small and represent the edge of their global geographical distribution. At a local scale, using long-term data (14 years) on annual breeding success and capture-resights of marked individuals, we estimated and compared the vital rates and evaluated the connectivity of two Spanish populations (Ebro Delta and Doñana) varying in their local environmental conditions. At a metapopulation scale, we analyzed 22 years of data on breeding numbers to predict their future prospects by means of population demographic models. Local survival and breeding success of gulls from the Ebro Delta was lower than those from Doñana, which is likely the result of higher permanent emigration and/or winter mortality in the former. Gulls from the Ebro Delta wintered mostly in Mediterranean areas whereas those from Doñana did so in Atlantic coasts, where food availability is higher. Whereas adult local survival was constant, juvenile local survival showed temporal parallel variations between colonies, probably related to natal dispersal to other breeding colonies. Our results suggested that dispersal was higher at the Ebro Delta and gulls emigrating from their natal colonies settled preferentially in close patches. We found large fluctuations in breeding numbers among local populations probably related to the fact that the Slender-billed gull is a species adapted to unstable and unpredictable habitats with high abilities to disperse between suitable patches depending on environmental stochastic conditions during breeding.

Adapting to a changing world: unraveling the role of man-made habitats as alternative feeding areas for slender-billed gull (Chroicocephalus genei).

Current rates of wildlife habitat loss have placed increasing demands on managers to develop, validate and implement tools aimed at improving our ability to evaluate such impacts on wildlife. Here, we present a case study conducted at the Natural Area of Doñana (SW Spain) where remote sensing and stable isotope (δ(13)C, δ(15)N) analyses of individuals were combined to unravel (1) the effect of variations in availability of natural food resources (i.e. from natural marshes) on reproductive performance of a Slender-billed Gull (Chroicocephalus genei) population, and (2) the role of two adjacent, artificial systems (a fish farm and saltmines) as alternate anthropogenic feeding areas. Based on long-term (1983-2004) remote-sensing, we inferred the average extent of flooded area at the marshland (a proxy to natural resource availability) annually. Estimated flooded areas (ranging from extreme drought [ca. 151 ha, 1995] to high moisture [15,049 ha, 2004]) were positively related to reproductive success of gulls (estimated for the 1993-2004 period, and ranging from ca. 0 to 1.7 fledglings per breeding pairs), suggesting that habitat availability played a role in determining their reproductive performance. Based on blood δ(13)C and δ(15)N values of fledglings, 2001-2004, and a Bayesian isotopic mixing model, we conclude that saltmines acted as the main alternative foraging habitat for gulls, with relative contributions increasing as the extent of marshland decreased. Although adjacent, anthropogenic systems have been established as the preferred breeding sites for this gull population, dietary switches towards exploitation of alternative (anthropogenic) food resources negatively affected the reproductive output of this species, thus challenging the perception that these man-made systems are necessarily a reliable buffer against loss of natural feeding habitats. The methodology and results derived from this study could be extended to a large suite of threatened natural communities worldwide, thus providing a useful framework for management and conservation.